Multiple mechanisms explain loss of anthocyanins from betalain-pigmented Caryophyllales, including repeated wholesale loss of a key anthocyanidin synthesis enzyme

Boas Pucker, Nathanael Walker-Hale, Jasmina Dzurlic, Won C. Yim, John C. Cushman, Alexandra Crum, Ya Yang, Samuel F. Brockington

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

In this study, we investigate the genetic mechanisms responsible for the loss of anthocyanins in betalain-pigmented Caryophyllales, considering our hypothesis of multiple transitions to betalain pigmentation. Utilizing transcriptomic and genomic datasets across 357 species and 31 families, we scrutinize 18 flavonoid pathway genes and six regulatory genes spanning four transitions to betalain pigmentation. We examined evidence for hypotheses of wholesale gene loss, modified gene function, altered gene expression, and degeneration of the MBW (MYB-bHLH-WD40) trasnscription factor complex, within betalain-pigmented lineages. Our analyses reveal that most flavonoid synthesis genes remain conserved in betalain-pigmented lineages, with the notable exception of TT19 orthologs, essential for the final step in anthocyanidin synthesis, which appear to have been repeatedly and entirely lost. Additional late-stage flavonoid pathway genes upstream of TT19 also manifest strikingly reduced expression in betalain-pigmented species. Additionally, we find repeated loss and alteration in the MBW transcription complex essential for canonical anthocyanin synthesis. Consequently, the loss and exclusion of anthocyanins in betalain-pigmented species appear to be orchestrated through several mechanisms: loss of a key enzyme, downregulation of synthesis genes, and degeneration of regulatory complexes. These changes have occurred iteratively in Caryophyllales, often coinciding with evolutionary transitions to betalain pigmentation.

Original languageEnglish (US)
Pages (from-to)471-489
Number of pages19
JournalNew Phytologist
Volume241
Issue number1
DOIs
StatePublished - Jan 2024

Bibliographical note

Publisher Copyright:
© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation.

Keywords

  • AN9
  • MBW complex
  • PAP1
  • TT19
  • anthocyanin biosynthesis
  • betalain biosynthesis
  • flavonoid biosynthesis
  • pigment evolution

PubMed: MeSH publication types

  • Journal Article

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